Assessing circulating tumour DNA (ctDNA) as a prognostic biomarker in locally advanced rectal cancer: a systematic review and meta-analysis.
Rectal cancer
Recurrence
Survival
ctDNA
Journal
International journal of colorectal disease
ISSN: 1432-1262
Titre abrégé: Int J Colorectal Dis
Pays: Germany
ID NLM: 8607899
Informations de publication
Date de publication:
29 May 2024
29 May 2024
Historique:
accepted:
23
05
2024
medline:
29
5
2024
pubmed:
29
5
2024
entrez:
29
5
2024
Statut:
epublish
Résumé
Circulating tumour DNA (ctDNA) has emerged as a promising biomarker in various cancer types, including locally advanced rectal cancer (LARC), offering potential insights into disease progression, treatment response and recurrence. This review aims to comprehensively evaluate the utility of ctDNA as a prognostic biomarker in LARC. PubMed, EMBASE and Web of Science were searched as part of our review. Studies investigating the utility of ctDNA in locally advanced rectal cancer (LARC) were assessed for eligibility. Quality assessment of included studies was performed using the Newcastle Ottawa Scale (NOS) risk of bias tool. Outcomes extracted included basic participant characteristics, ctDNA details and survival data. A meta-analysis was performed on eligible studies to determine pooled recurrence-free survival (RFS). Twenty-two studies involving 1676 participants were included in our analysis. Methodological quality categorised by the Newcastle Ottawa Scale was generally satisfactory across included studies. ctDNA detected at various time intervals was generally associated with poor outcomes across included studies. Meta-analysis demonstrated a pooled hazard ratio of 8.87 (95% CI 4.91-16.03) and 15.15 (95% CI 8.21-27.95), indicating an increased risk of recurrence with ctDNA positivity in the post-neoadjuvant and post-operative periods respectively. Our systematic review provides evidence supporting the prognostic utility of ctDNA in patients with LARC, particularly in identifying patients at higher risk of disease recurrence in the post-neoadjuvant and post-operative periods.
Identifiants
pubmed: 38809315
doi: 10.1007/s00384-024-04656-1
pii: 10.1007/s00384-024-04656-1
doi:
Substances chimiques
Circulating Tumor DNA
0
Biomarkers, Tumor
0
Types de publication
Systematic Review
Meta-Analysis
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
82Informations de copyright
© 2024. The Author(s).
Références
Kokelaar RF, Evans MD, Davies M, Harris DA, Beynon J (2016) Locally advanced rectal cancer: management challenges. Onco Targets Ther 9:6265–6272
pubmed: 27785074
pmcid: 5066998
doi: 10.2147/OTT.S100806
Smith JJ, Garcia-Aguilar J (2015) Advances and challenges in treatment of locally advanced rectal cancer. J Clin Oncol 33(16):1797–1808
pubmed: 25918296
pmcid: 4559608
doi: 10.1200/JCO.2014.60.1054
Ryan EJ, Creavin B, Sheahan K (2020) Delivery of personalized care for locally advanced rectal cancer: incorporating pathological, molecular genetic, and immunological biomarkers into the multimodal paradigm. Front Oncol 10:1369
pubmed: 32923389
pmcid: 7456909
doi: 10.3389/fonc.2020.01369
Chen C, Douglas MP, Ragavan MV, Phillips KA, Jansen JP (2023) Clinical validity and utility of circulating tumor DNA (ctDNA) testing in advanced non-small cell lung cancer (aNSCLC): a systematic literature review and meta-analysis. medRxiv [Preprint]. https://doi.org/10.1101/2023.10.27.23297657 (PMID: 37961510; PMCID: PMC10635208)
doi: 10.1101/2023.10.27.23297657
Guven DC, Sahin TK, Yildirim HC, Aktepe OH, Dizdar O, Yalcin S (2021) A systematic review and meta-analysis of the association between circulating tumor DNA (ctDNA) and prognosis in pancreatic cancer. Crit Rev Oncol Hematol 168:103528
pubmed: 34800650
doi: 10.1016/j.critrevonc.2021.103528
Wullaert L, van Rees JM, Martens JWM, Verheul HMW, Grünhagen DJ, Wilting SM, Verhoef C (2023) Circulating tumour DNA as biomarker for colorectal liver metastases: a systematic review and meta-analysis. Cells 12(21):2520. https://doi.org/10.3390/cells12212520 (PMID: 37947598; PMCID: PMC10647834)
doi: 10.3390/cells12212520
pubmed: 37947598
pmcid: 10647834
Sun X, Abrahamson P, Ballew N, Kalilani L, Phiri K, Bell KF et al (2023) The utility of ctDNA in lung cancer clinical research and practice: a systematic review and meta-analysis of clinical studies. Cancer Invest 41(6):571–592
pubmed: 37272675
doi: 10.1080/07357907.2023.2220820
Dizdarevic E, Hansen TF, Jakobsen A (2022) The prognostic importance of ctDNA in rectal cancer: a critical reappraisal. Cancers 14(9):2252. https://doi.org/10.3390/cancers14092252 (PMID: 35565381; PMCID: PMC9101261)
doi: 10.3390/cancers14092252
pubmed: 35565381
pmcid: 9101261
Pessoa LS, Heringer M, Ferrer VP (2020) ctDNA as a cancer biomarker: a broad overview. Crit Rev Oncol Hematol 155:103109
pubmed: 33049662
doi: 10.1016/j.critrevonc.2020.103109
Gorgannezhad L, Umer M, Islam MN, Nguyen NT, Shiddiky MJA (2018) Circulating tumor DNA and liquid biopsy: opportunities, challenges, and recent advances in detection technologies. Lab Chip 18(8):1174–1196
pubmed: 29569666
doi: 10.1039/C8LC00100F
Lebofsky R, Decraene C, Bernard V, Kamal M, Blin A, Leroy Q et al (2015) Circulating tumor DNA as a non-invasive substitute to metastasis biopsy for tumor genotyping and personalized medicine in a prospective trial across all tumor types. Mol Oncol 9(4):783–790
pubmed: 25579085
doi: 10.1016/j.molonc.2014.12.003
Postel M, Roosen A, Laurent-Puig P, Taly V, Wang-Renault SF (2018) Droplet-based digital PCR and next generation sequencing for monitoring circulating tumor DNA: a cancer diagnostic perspective. Expert Rev Mol Diagn 18(1):7–17
pubmed: 29115895
doi: 10.1080/14737159.2018.1400384
Satam H, Joshi K, Mangrolia U, Waghoo S, Zaidi G, Rawool S, Thakare RP, Banday S, Mishra AK, Das G, Malonia SK (2023) Next-generation sequencing technology: current trends and advancements. Biology 12(7):997. https://doi.org/10.3390/biology12070997 (Erratum in: Biology (Basel). 2024 Apr 24;13(5): PMID: 37508427; PMCID: PMC10376292)
doi: 10.3390/biology12070997
pubmed: 37508427
pmcid: 10376292
Gezer U, Bronkhorst AJ, Holdenrieder S (2022) The clinical utility of droplet digital PCR for profiling circulating tumor DNA in breast cancer patients. Diagnostics 12(12):3042. https://doi.org/10.3390/diagnostics12123042 (PMID: 36553049; PMCID: PMC9776872)
doi: 10.3390/diagnostics12123042
pubmed: 36553049
pmcid: 9776872
Dymond JS (2013) Explanatory chapter: quantitative PCR. Methods Enzymol 529:279–289
pubmed: 24011054
doi: 10.1016/B978-0-12-418687-3.00023-9
Nakamura K (2016) Circulating Tumor DNA (ctDNA) Detection using BEAMing and its clinical significance. Rinsho Byori 64(4):400–6
pubmed: 29182806
Mouliere F, Chandrananda D, Piskorz AM, Moore EK, Morris J, Ahlborn LB, Mair R, Goranova T, Marass F, Heider K, Wan JCM, Supernat A, Hudecova I, Gounaris I, Ros S, Jimenez-Linan M, Garcia-Corbacho J, Patel K, Østrup O, Murphy S, Eldridge MD, Gale D, Stewart GD, Burge J, Cooper WN, van der Heijden MS, Massie CE, Watts C, Corrie P, Pacey S, Brindle KM, Baird RD, Mau-Sørensen M, Parkinson CA, Smith CG, Brenton JD, Rosenfeld N (2018) Enhanced detection of circulating tumor DNA by fragment size analysis. Sci Transl Med 10(466):eaat4921. https://doi.org/10.1126/scitranslmed.aat4921 (PMID: 30404863; PMCID: PMC6483061)
doi: 10.1126/scitranslmed.aat4921
pubmed: 30404863
pmcid: 6483061
Khatami F, Tavangar SM (2018) Circulating tumor DNA (ctDNA) in the era of personalized cancer therapy. J Diabetes Metab Disord 17(1):19–30
pubmed: 30288382
pmcid: 6154523
doi: 10.1007/s40200-018-0334-x
Martín-Carnicero A, Ramalle-Gomara E, Rubio-Mediavilla S, Alonso-Lago M, Zorrilla-Larraga M, Manrique-Abós I, de las Heras-Dueña ME, Larrayoz IM, Martínez A (2022) Prognostic and predictive biomarkers in patients with Locally Advanced Rectal Cancer (LARC) treated with preoperative chemoradiotherapy. J Clin Med 11:6091. https://doi.org/10.3390/jcm11206091
doi: 10.3390/jcm11206091
pubmed: 36294412
pmcid: 9604791
Valenza C, Trapani D, Curigliano G (2022) Circulating tumour DNA dynamics for assessment of molecular residual disease and for intercepting resistance in breast cancer. Curr Opin Oncol 34(6):595–605
pubmed: 36083118
doi: 10.1097/CCO.0000000000000905
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372:n71
pubmed: 33782057
pmcid: 8005924
doi: 10.1136/bmj.n71
Covidence systematic review software. Veritas Health Innovation, Melbourne, Australia
Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25(9):603–605
pubmed: 20652370
doi: 10.1007/s10654-010-9491-z
Hozo SP, Djulbegovic B, Hozo I (2005) Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 5:13
pubmed: 15840177
pmcid: 1097734
doi: 10.1186/1471-2288-5-13
Agostini M, Pucciarelli S, Enzo MV, Del Bianco P, Briarava M, Bedin C et al (2011) Circulating cell-free DNA: a promising marker of pathologic tumor response in rectal cancer patients receiving preoperative chemoradiotherapy. Ann Surg Oncol 18(9):2461–2468
pubmed: 21416156
doi: 10.1245/s10434-011-1638-y
Alden SL, Lee V, Narang AK, Meyer J, Gearhart SL, Christenson ES (2024) Circulating tumor DNA to predict radiographic and pathologic response to total neoadjuvant therapy in locally advanced rectal cancer. Oncologist 29(3):e414–e418
pubmed: 38180954
pmcid: 10911913
doi: 10.1093/oncolo/oyad336
Appelt AL, Andersen RF, Lindebjerg J, Jakobsen A (2020) Prognostic value of serum NPY hypermethylation in neoadjuvant chemoradiotherapy for rectal cancer: secondary analysis of a randomized trial. Am J Clin Oncol 43(1):9–13
pubmed: 31569168
doi: 10.1097/COC.0000000000000609
Boysen AK, Wettergren Y, Sorensen BS, Taflin H, Gustavson B, Spindler KG (2017) Cell-free DNA levels and correlation to stage and outcome following treatment of locally advanced rectal cancer. Tumour Biol 39(11):1010428317730976
pubmed: 29110585
doi: 10.1177/1010428317730976
Guo ZW, Xiao WW, Yang XX, Yang X, Cai GX, Wang XJ et al (2020) Noninvasive prediction of response to cancer therapy using promoter profiling of circulating cell-free DNA. Clin Transl Med 10(5):e174
pubmed: 32997420
pmcid: 7507006
doi: 10.1002/ctm2.174
Hofste LSM, Geerlings MJ, von Rhein D, Rutten H, Westenberg AH, Weiss MM et al (2023) Circulating tumor DNA detection after neoadjuvant treatment and surgery predicts recurrence in patients with early-stage and locally advanced rectal cancer. Eur J Surg Oncol 49(7):1283–1290
pubmed: 36740555
doi: 10.1016/j.ejso.2023.01.026
Jiang XF, Zhang BM, Du FQ, Guo JN, Wang D, Li YE et al (2022) Exploring biomarkers for prognosis and neoadjuvant chemosensitivity in rectal cancer: multi-omics and ctDNA sequencing collaboration. Front Immunol 13:1013828
pubmed: 36569844
pmcid: 9780298
doi: 10.3389/fimmu.2022.1013828
Khakoo S, Carter PD, Brown G, Valeri N, Picchia S, Bali MA et al (2020) MRI tumor regression grade and circulating tumor DNA as complementary tools to assess response and guide therapy adaptation in rectal cancer. Clin Cancer Res 26(1):183–192
pubmed: 31852830
doi: 10.1158/1078-0432.CCR-19-1996
Liu W, Li Y, Tang Y, Song Q, Wang J, Li N et al (2022) Response prediction and risk stratification of patients with rectal cancer after neoadjuvant therapy through an analysis of circulating tumour DNA. EBioMedicine 78:103945
pubmed: 35306340
pmcid: 8933829
doi: 10.1016/j.ebiom.2022.103945
McDuff SGR, Hardiman KM, Ulintz PJ, Parikh AR, Zheng H, Kim DW, Lennerz JK, Hazar-Rethinam M, Van Seventer EE, Fetter IJ, Nadres B, Eyler CE, Ryan DP, Weekes CD, Clark JW, Cusack JC, Goyal L, Zhu AX, Wo JY, Blaszkowsky LS, Allen J, Corcoran RB, Hong TS (2021) Circulating tumor DNA predicts pathologic and clinical outcomes following neoadjuvant chemoradiation and surgery for patients with locally advanced rectal cancer. JCO Precis Oncol 5:123–132. https://doi.org/10.1200/PO.20.00220 (PMID: 34250394; PMCID: PMC8232395)
doi: 10.1200/PO.20.00220
Morais M, Fonseca T, Melo-Pinto D, Prieto I, Vilares AT, Duarte AL, Leitão P, Cirnes L, Machado JC, Carneiro S (2023) Evaluation of ctDNA in the prediction of response to neoadjuvant therapy and prognosis in locally advanced rectal cancer patients: a prospective study. Pharmaceuticals 16(3):427. https://doi.org/10.3390/ph16030427 (PMID: 36986526; PMCID: PMC10057108)
doi: 10.3390/ph16030427
pubmed: 36986526
pmcid: 10057108
Murahashi S, Akiyoshi T, Sano T, Fukunaga Y, Noda T, Ueno M et al (2020) Serial circulating tumour DNA analysis for locally advanced rectal cancer treated with preoperative therapy: prediction of pathological response and postoperative recurrence. Br J Cancer 123(5):803–810
pubmed: 32565539
pmcid: 7462982
doi: 10.1038/s41416-020-0941-4
Pazdirek F, Minarik M, Benesova L, Halkova T, Belsanova B, Macek M et al (2020) Monitoring of early changes of circulating tumor DNA in the plasma of rectal cancer patients receiving neoadjuvant concomitant chemoradiotherapy: evaluation for prognosis and prediction of therapeutic response. Front Oncol 10:1028
pubmed: 32793464
pmcid: 7394215
doi: 10.3389/fonc.2020.01028
Roesel R, Epistolio S, Molinari F, Saletti P, De Dosso S, Valli M et al (2022) A pilot, prospective, observational study to investigate the value of NGS in liquid biopsies to predict tumor response after neoadjuvant chemo-radiotherapy in patients with locally advanced rectal cancer: the LiBReCa study. Front Oncol 12:900945
pubmed: 35837093
pmcid: 9274270
doi: 10.3389/fonc.2022.900945
Schou JV, Larsen FO, Sorensen BS, Abrantes R, Boysen AK, Johansen JS et al (2018) Circulating cell-free DNA as predictor of treatment failure after neoadjuvant chemo-radiotherapy before surgery in patients with locally advanced rectal cancer. Ann Oncol 29(3):610–615
pubmed: 29253083
doi: 10.1093/annonc/mdx778
Sclafani F, Chau I, Cunningham D, Hahne JC, Vlachogiannis G, Eltahir Z et al (2018) KRAS and BRAF mutations in circulating tumour DNA from locally advanced rectal cancer. Sci Rep 8(1):1445
pubmed: 29362371
pmcid: 5780472
doi: 10.1038/s41598-018-19212-5
Sun W, Sun Y, Zhu M, Wang Z, Zhang H, Xin Y et al (2014) The role of plasma cell-free DNA detection in predicting preoperative chemoradiotherapy response in rectal cancer patients. Oncol Rep 31(3):1466–1472
pubmed: 24378613
doi: 10.3892/or.2013.2949
Tie J, Cohen JD, Wang Y, Li L, Christie M, Simons K et al (2019) Serial circulating tumour DNA analysis during multimodality treatment of locally advanced rectal cancer: a prospective biomarker study. Gut 68(4):663–671
pubmed: 29420226
doi: 10.1136/gutjnl-2017-315852
Truelsen CG, Kronborg CS, Sorensen BS, Callesen LB, Spindler KG (2022) Circulating cell-free DNA as predictor of pathological complete response in locally advanced rectal cancer patients undergoing preoperative chemoradiotherapy. Clin Transl Radiat Oncol 36:9–15
pubmed: 35733829
pmcid: 9207192
Vidal J, Casadevall D, Bellosillo B, Pericay C, Garcia-Carbonero R, Losa F et al (2021) Clinical impact of presurgery circulating tumor DNA after total neoadjuvant treatment in locally advanced rectal cancer: a biomarker study from the GEMCAD 1402 trial. Clin Cancer Res 27(10):2890–2898
pubmed: 33727257
doi: 10.1158/1078-0432.CCR-20-4769
Wang Y, Yang L, Bao H, Fan X, Xia F, Wan J et al (2021) Utility of ctDNA in predicting response to neoadjuvant chemoradiotherapy and prognosis assessment in locally advanced rectal cancer: a prospective cohort study. PLoS Med 18(8):e1003741
pubmed: 34464382
pmcid: 8407540
doi: 10.1371/journal.pmed.1003741
Zhou J, Wang C, Lin G, Xiao Y, Jia W, Xiao G et al (2021) Serial circulating tumor DNA in predicting and monitoring the effect of neoadjuvant chemoradiotherapy in patients with rectal cancer: a prospective multicenter study. Clin Cancer Res 27(1):301–310
pubmed: 33046514
doi: 10.1158/1078-0432.CCR-20-2299
Chan HT, Nagayama S, Otaki M, Chin YM, Fukunaga Y, Ueno M et al (2022) Tumor-informed or tumor-agnostic circulating tumor DNA as a biomarker for risk of recurrence in resected colorectal cancer patients. Front Oncol 12:1055968
pubmed: 36776372
doi: 10.3389/fonc.2022.1055968
Parikh AR, Van Seventer EE, Siravegna G, Hartwig AV, Jaimovich A, He Y et al (2021) Minimal residual disease detection using a plasma-only circulating tumor DNA assay in patients with colorectal cancer. Clin Cancer Res 27(20):5586–5594
pubmed: 33926918
pmcid: 8530842
doi: 10.1158/1078-0432.CCR-21-0410
Gong J, Hendifar A, Gangi A, Zaghiyan K, Atkins K, Nasseri Y, Murrell Z, Figueiredo JC, Salvy S, Haile R, Hitchins M (2021) Clinical applications of minimal residual disease assessments by tumor-informed and tumor-uninformed circulating tumor DNA in colorectal cancer. Cancers 13(18):4547. https://doi.org/10.3390/cancers13184547 (PMID: 34572774; PMCID: PMC8471730)
doi: 10.3390/cancers13184547
pubmed: 34572774
pmcid: 8471730
Tie J, Wang Y, Tomasetti C, Li L, Springer S, Kinde I et al (2016) Circulating tumor DNA analysis detects minimal residual disease and predicts recurrence in patients with stage II colon cancer. Sci Transl Med 8(346):346ra92
pubmed: 27384348
pmcid: 5346159
doi: 10.1126/scitranslmed.aaf6219
Tie J, Cohen JD, Wang Y, Ginestet PG, Wong R, Shapiro JD et al (2024) Circulating tumor DNA analysis informing adjuvant chemotherapy in locally advanced rectal cancer: the randomized AGITG DYNAMIC-Rectal study. J Clin Oncol 42(3_suppl):12
doi: 10.1200/JCO.2024.42.3_suppl.12
Dang DK, Park BH (2022) Circulating tumor DNA: current challenges for clinical utility. J Clin Invest. 132(12):e154941. https://doi.org/10.1172/JCI154941 (PMID: 35703177; PMCID: PMC9197509)
doi: 10.1172/JCI154941
pubmed: 35703177
pmcid: 9197509
Spoor J, Eyck BM, Atmodimedjo PN, Jansen M, Helmijr JCA, Martens JWM et al (2021) Liquid biopsy in esophageal cancer: a case report of false-positive circulating tumor DNA detection due to clonal hematopoiesis. Ann Transl Med 9(15):1264
pubmed: 34532401
pmcid: 8421960
doi: 10.21037/atm-21-525
Allan Z, Liu DS, Lee MM, Tie J, Clemons NJ (2024) A practical approach to interpreting circulating tumor DNA in the management of gastrointestinal cancers. Clin Chem 70(1):49–59
pubmed: 38175583
doi: 10.1093/clinchem/hvad188
Wehrle J, Philipp U, Jolic M, Follo M, Hussung S, Waldeck S, Deuter M, Rassner M, Braune J, Rawluk J, Greil C, Waller CF, Becker H, Duque-Afonso J, Illert AL, Fritsch RM, Meiss F, Duyster J, von Bubnoff N, Scherer F (2020) Personalized treatment selection and disease monitoring using circulating tumor DNA profiling in real-world cancer patient management. Diagnostics 10(8):550. https://doi.org/10.3390/diagnostics10080550 (PMID: 32748806; PMCID: PMC7459590)
doi: 10.3390/diagnostics10080550
pubmed: 32748806
pmcid: 7459590
Sanchez-Herrero E, Serna-Blasco R, Robado de Lope L, Gonzalez-Rumayor V, Romero A, Provencio M (2022) Circulating tumor DNA as a cancer biomarker: an overview of biological features and factors that may impact on ctDNA analysis. Front Oncol 12:943253
pubmed: 35936733
pmcid: 9350013
doi: 10.3389/fonc.2022.943253
Stadler JC, Belloum Y, Deitert B, Sementsov M, Heidrich I, Gebhardt C et al (2022) Current and future clinical applications of ctDNA in immuno-oncology. Cancer Res 82(3):349–358
pubmed: 34815256
doi: 10.1158/0008-5472.CAN-21-1718
Cree IA, Indave Ruiz BI, Zavadil J, McKay J, Olivier M, Kozlakidis Z et al (2021) The international collaboration for cancer classification and research. Int J Cancer 148(3):560–571
pubmed: 32818326
doi: 10.1002/ijc.33260